The Journal of Experimental Medicine
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Published online 27 January 2003 doi:10.1084/jem.20021639
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© Rockefeller University Press, 0022-1007/2003/2/333 $5.00
The Journal of Experimental Medicine, Volume 197, Number 3, 333-341

Extrathymic T Cell Lymphopoiesis : Ontogeny and Contribution to Gut Intraepithelial Lymphocytes in Athymic and Euthymic Mice



Delphine Guy-Grand1, Orly Azogui1, Susanna Celli1, Sylvie Darche1, Michel C. Nussenzweig2, Philippe Kourilsky1 and Pierre Vassalli3

1 Unité de Biologie Moléculaire du Gène, INSERM U277 and Institut Pasteur, 75724 Paris Cedex 15, France
2 Laboratory of Molecular Immunology, Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10021
3 Département de Pathologie, Centre Médical Universitaire, CH-1211, Genève 4, Switzerland

Address correspondence to Delphine Guy-Grand, Unité de Biologie Moléculaire du Gène, INSERM U277 and Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France. Phone: 33-1-40-61-32-09; Fax: 33-1-45-68-85-48; E-mail: guygrand{at}pasteur.fr; or Pierre Vassalli, Département de Pathologie, Centre Médical Universitaire, 1 rue Michel Servet, CH-1211, Genève 4, Switzerland. Phone: 41-22-347-56-30; Fax: 41-22-347-56-41; E-mail: pierre.vassalli{at}medecine.unige.ch

In the absence of thymopoiesis, T lymphocytes are nevertheless present, mainly in the gut epithelium. Ontogeny of the extrathymic pathway and the extent of its involvement in euthymic mice are controversial. These questions have been addressed by assessing the expression of recombinase activating gene (RAG) through the use of green fluorescent protein RAG2 transgenic mouse models. In athymic mice, T lymphopoiesis occurs mainly in the mesenteric lymph node and less in the Peyer's patches. Ontogenic steps of this lymphopoiesis resemble those of thymopoiesis, but with an apparent bias toward {gamma}{delta} T cell production and with a paucity of oligoclonal {alpha}ß T cells possibly resulting from a deficit in positive selection. Whether in athymic or euthymic mice, neither T intraepithelial lymphocytes (IEL) nor cryptopatch cells (reported to contain precursors of IEL) displayed fluorescence indicating recent RAG protein synthesis. Newly made T cells migrate from the mesenteric node into the thoracic duct lymph to reach the gut mucosa. In euthymic mice, this extrathymic pathway is totally repressed, except in conditions of severe lymphocytic depletion. Thus, in normal animals, all gut T IEL, including CD8{alpha}{alpha}+ cells, are of thymic origin, CD8{alpha}{alpha}+ TCR{alpha}ß+ IEL being the likely progeny of double negative NK1-1- thymocytes, which show polyclonal V{alpha} and Vß repertoires.

Key Words: T lymphocytes • extrathymic differentiation • gut intraepithelial lymphocytes • recombinase activating gene • mucosal immunity


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